1887

Abstract

Apoptosis induction of host macrophages has emerged as a common virulence mechanism among bacterial pathogens. Infection with is a leading cause of gastroenteritis worldwide and is characterized by an acute inflammatory response in the small intestine. The authors used the human monocytic cell line THP-1 to examine apoptosis induction and pro-inflammatory cytokine production during infection. Flow cytometric analysis revealed that 48 h after inoculation, a wild-type isolate induced apoptosis in 63 % of THP-1 cells while only 34 % of cells inoculated with a mutant, which does not secrete the Cia ( invasion antigens) proteins, underwent apoptosis. Complementation of the mutant resulted in levels of apoptosis similar to those induced by the wild-type isolate, suggesting that the Cia proteins have a role in apoptosis induction. It was shown that a proteinase K- and heat-stable component of also stimulated THP-1 apoptosis. Inoculation with a mutant indicated that lipooligosaccharide was not the stimulatory molecule. Immunoblot and ELISA analyses revealed that infection stimulated the synthesis, processing and secretion of interleukin 1 (IL-1). Inhibition of caspase 1 activity eliminated IL-1 processing and secretion, but did not affect apoptosis induction. In addition, treatment of cells with a caspase-9-specific inhibitor did not affect apoptosis induction, arguing against activation of an apoptotic pathway dependent on either caspase 1 or 9 activation. Collectively, these data suggest that the inoculation of macrophages with results in the processing of IL-1 and apoptosis through different regulatory pathways. Furthermore, these data argue that may use a mechanism distinct from and to initiate macrophage apoptosis and release of IL-1.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26466-0
2004-03-01
2020-07-13
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/3/mic1500561.html?itemId=/content/journal/micro/10.1099/mic.0.26466-0&mimeType=html&fmt=ahah

References

  1. Andrei C., Dazzi C., Lotti L., Torrisi M. R., Chimini G., Rubartelli A.. 1999; The secretory route of the leaderless protein interleukin 1β involves exocytosis of endolysosome-related vesicles. Mol Biol Cell10:1463–1475[CrossRef]
    [Google Scholar]
  2. Bacon D. J., Szymanski C. M., Burr D. H., Silver R. P., Alm R. A., Guerry P.. 2001; A phase-variable capsule is involved in virulence of Campylobacter jejuni 81-176. Mol Microbiol40:769–777[CrossRef]
    [Google Scholar]
  3. Chen Y., Smith M. R., Thirumalai K., Zychlinsky A.. 1996; A bacterial invasin induces macrophage apoptosis by binding directly to ICE. EMBO J15:3853–3860
    [Google Scholar]
  4. Day J. W. A., Sajecki J. L., Pitts T. M., Joens L. A.. 2000; Role of catalase in Campylobacter jejuni intracellular survival. Infect Immun68:6337–6345[CrossRef]
    [Google Scholar]
  5. Hersh D., Monack D. M., Smith M. R., Ghori N., Falkow S., Zychlinsky A.. 1999; The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci U S A96:2396–2401[CrossRef]
    [Google Scholar]
  6. Johnson W. M., Lior H.. 1988; A new heat-labile cytolethal distending toxin (CLDT) produced by Campylobacter spp. Microbial Pathog4:115–126[CrossRef]
    [Google Scholar]
  7. Jones M. A., Tötemeyer S., Maskell D. J., Bryant C. E., Barrow P. A.. 2003; Induction of proinflammatory responses in the human monocytic cell line THP-1 by Campylobacter jejuni. Infect Immun71:2626–2633[CrossRef]
    [Google Scholar]
  8. Karlyshev A., Linton D., Gregson N. A., Lastovica A. J., Wren B. W.. 2000; Genetic and biochemical evidence of a Campylobacter jejuni capsular polysaccharide that accounts for Penner serotype specificity. Mol Microbiol35:529–541
    [Google Scholar]
  9. Konkel M. E., Mead D. J., Hayes S. F., Cieplak W.. 1992; Translocation of Campylobacter jejuni across human polarized epithelial cell monolayer cultures. J Infect Dis166:308–315[CrossRef]
    [Google Scholar]
  10. Konkel M. E., Kim B. J., Rivera-Amill V., Garvis S. G.. 1999; Bacterial secreted proteins are required for the internalization of Campylobacter jejuni into cultured mammalian cells. Mol Microbiol32:691–702[CrossRef]
    [Google Scholar]
  11. Konkel M. E., Monteville M. R., Rivera-Amill V., Joens L. A.. 2001; The pathogenesis of Campylobacter jejuni-mediated enteritis. Curr Issues Intest Microbiol2:55–71
    [Google Scholar]
  12. Li L. Y., Luo X., Wang X.. 2001; Endonuclease G is an apoptotic DNase when released from the mitochondria. Nature412:95–99[CrossRef]
    [Google Scholar]
  13. Logan S. M., Trust T. J.. 1984; Structural and antigenic heterogeneity of lipopolysaccharides of Campylobacter jejuni and Campylobacter coli. Infect Immun45:210–216
    [Google Scholar]
  14. Marsden V. S., O'Connor L., O'Reilly L. A..13 other authors 2002; Apoptosis initiated by Bcl-2-regulated caspase activation independently of the cytochrome c/Apaf-1/caspase-9 apoptosome. Nature419:634–637[CrossRef]
    [Google Scholar]
  15. Mead P. S., Slutsker L., Kietz V., McCaig L. F., Bresee J. S., Shapiro C., Griffin P. M., Tauxe R. T.. 1999; Food-related illness and death in the United States. Emerg Infect Dis5:607–625[CrossRef]
    [Google Scholar]
  16. Monack D. M., Raupach B., Hromockyj A., Falkow S.. 1996; Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc Natl Acad Sci U S A93:9833–9838[CrossRef]
    [Google Scholar]
  17. Monack D. M., Mecsas J., Ghori N., Falkow S.. 1997; Yersinia signals macrophages to undergo apoptosis and YopJ is necessary for this cell death. Proc Natl Acad Sci U S A94:10385–10390[CrossRef]
    [Google Scholar]
  18. Navarre W. W., Zychlinsky A.. 2000; Pathogen-induced apoptosis of macrophages: a common end for different pathogenic strategies. Cell Microbiol2:265–273[CrossRef]
    [Google Scholar]
  19. Nikaido H., Vaara M.. 1985; Molecular basis of bacterial outer membrane permeability. Microbiol Rev49:1–32
    [Google Scholar]
  20. Oldfield N. J., Moran A. P., Millar L. A., Prendergast M. M., Ketley J. M.. 2002; Characterization of the Campylobacter jejuni heptosyltransferase II gene, waaF, provides genetic evidence that extracellular polysaccharide is lipid A core independent. J Bacteriol184:2100–2107[CrossRef]
    [Google Scholar]
  21. Rivera-Amill V., Kim B. J., Seshu J., Konkel M. E.. 2001; Secretion of the virulence-associated Campylobacter invasion antigens from Campylobacter jejuni requires a stimulatory signal. J Infect Dis183:1607–1616[CrossRef]
    [Google Scholar]
  22. Ruckdeschel K., Mannel O., Richter K., Heesemann J., Jacobi C. A., Trülzsch K., Rouot B.. 2001; Yersinia outer protein P of Yersinia enterocolitica simultaneously blocks the nuclear factor-κB pathway and exploits lipopolysaccharide signaling to trigger apoptosis in macrophages. J Immunol166:1823–1831[CrossRef]
    [Google Scholar]
  23. Sirisena D. M., MacLachlan P. R., Liu S. L., Hessel A., Sanderson K. E.. 1994; Molecular analysis of the rfaD gene, for heptose synthesis,and the rfaF gene, for heptose transfer, in lipopolysaccharide synthesis in Salmonella typhimurium. J Bacteriol176:2379–2385
    [Google Scholar]
  24. Tschopp J., Martinon F., Burns K.. 2003; NALPS: a novel protein family involved in inflammation. Mol Cell Biol4:95–104
    [Google Scholar]
  25. Tsuchiya S., Kobayashi Y., Goto H., Okumura S., Nakae T., Konmo T., Tada K.. 1982; Induction of maturation in cultured human monocytic leukemia cells by phorbol ester. Cancer Res42:1530–1536
    [Google Scholar]
  26. Valvano M. A., Marolda C. L., Bittner M., Glaskin-Clay M., Simon T. L., Klena J. D.. 2000; The rfaE gene from Escherichia coli encodes a bifunctional protein involved in biosynthesis of the lipopolysaccharide core precursor ADP-l-glycero-d-manno-heptose. J Bacteriol182:488–497[CrossRef]
    [Google Scholar]
  27. Zhu J., Meinersmann R. J., Hiett K. L., Evans D. L.. 1999; Apoptotic effect of outer-membrane proteins from Campylobacter jejuni on chicken lymphocytes. Curr Microbiol38:244–249[CrossRef]
    [Google Scholar]
  28. Zychlinsky A., Fitting C., Cavaillon J. M., Sansonetti P. J.. 1994; Interleukin 1 is released by murine macrophages during apoptosis induced by Shigella flexneri. J Clin Invest94:1328–1332[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.26466-0
Loading
/content/journal/micro/10.1099/mic.0.26466-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error